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 Handbook
of
Biochemistry
and
Molecular Biology
CRC Handbook
of
Biochemistry
and
Molecular
Biology
3rd Edition
Proteins - Volume III
Editor

Gerald D. Fasman, Ph.D.

Rosenfield Professor of Biochemistry
Graduate Department of Biochemistry
Brandeis University
Waltham, Massachusetts

Boca Raton London New York

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Taylor & Francis Group, an informa business
First published 1976 by CRC Press
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Reissued 2018 by CRC Press

© 1976 by Taylor & Francis

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 Handbook
of
Biochemistry
and
Molecular Biology
3rd Edition

Proteins —Volume III

Editor
Gerald D. Fasman, Ph. D.
Rosenfield Professor of Biochemistry
Graduate Department of Biochemistry
Brandeis University
Waltham, Massachusetts

The following is a list of the four major sections of the Handbook,

each consisting of one or more volumes

Proteins - Amino Acids, Peptides, Polypeptides, and Proteins

Nucleic, Acids — Purines, Pyrimidines, Nucleotides, Oligonucleotides,

tRNA, DNA, RNA

Lipids, Carbohydrates, Steroids

Physical and Chemical Data, Miscellaneous —Ion Exchange, Chromatog­

raphy, Buffers, Miscellaneous, e.g., Vitamins
 ADVI SORY BOARD

Gerald D. Fasman
Editor

Herbert A. Sober (deceased)

Consulting Editor

MEMBERS

Bruce Ames Victor Ginsburg

Professor, Department of Biochemistry Chief, Biochemistry Section, National
University of California Institute of Arthritis, Metabolism and
Berkeley, California 94720 Digestive Diseases
Department of Health, Education, and
Sherman Beychok Welfare
Professor, Department of Biological National Institutes of Health
Sciences Bethesda, Maryland 20014
Columbia University
New York, New York 10027
Walter Gratzer
MRC Neurobiology Unit
Waldo E. Cohn
Department of Biophysics
Senior Biochemist, Biology Division
Oak Ridge National Laboratory Kings College
University of London
Oak Ridge, Tennessee 37830
London
England
Harold Edelhoch
National Institute Arthritis, Metabolism
Lawrence Grossman
and Digestive Diseases
Department of Health, Education, and Professor, Department of Biochemical and
Welfare Biophysical Sciences
National Institutes of Health School of Hygiene and Public Health
Bethesda, Maryland 20014 The Johns Hopkins University
Baltimore, Maryland 21205
John Edsall
Professor Emeritus, Biological Laboratories Frank Gurd
Harvard University Professor, Department of Chemistry
Cambridge, Massachusetts 02138 Indiana University
Bloomington, Indiana 47401
Gary Felsenfeld
Chief, Physical Chemistry Laboratory
Laboratory of Molecular Biology William Harrington
National Institute of Arthritis, Professor, Department of Biology
Metabolism, and Digestive Diseases The Johns Hopkins University
National Institutes Of Health Baltimore, Maryland 21218
Bethesda, Maryland 20014
William P. Jencks
Edmond H. Fischer Professor, Graduate Department of
Professor, Department of Biochemistry Biochemistry
University of Washington Brandeis University
Seattle, Washington 98195 Waltham, Massachusetts 02154
 ADVISORY BOARD (continued)

0 . L. Kline Julius Marmur

Executive Officer Professor, Department of Biochemistry
American Institute of Nutrition and Genetics
9650 Rockville Pike Albert Einstein College of Medicine
Bethesda, Maryland 20014 New York, New York 10461

1. M. Klotz
Alton Meister
Professor, Department of Chemistry Professor, Department of Biochemistry
Northwestern University Cornell University Medical College
Evanston, Illinois 60201 New York, New York 10021

Robert Langridge
Professor, Department of Biochemistry Kivie Moldave
Princeton University Professor, Department of Biochemistry
Princeton, New Jersey 08540 California College of Medicine
University of California
Irvine, California 92664
Philip Leder
Chief, Laboratory of Molecular Genetics
National Institute of Child Health D. C. Phillips
and Human Development Professor, Laboratory of Molecular
National Institutes of Health Biophysics
Bethesda, Maryland 20014 Department of Zoology
Oxford University
1. Robert Lehman Oxford
Professor, Department Biochemistry England
School of Medicine
Stanford University William D. Phillips
Stanford, California 94305 The Lord Rank Research Centre
Ranks Hove, McDougall Ltd.
Lawrence Levine Lincoln Road, High Wycombe
Professor, Graduate Department of Bucks
Biochemistry England
Brandeis University
Waltham, Massachusetts 02154
G. N. Ramachandran
John Lowenstein Professor, Molecular Biophysics Unit
Professor, Graduate Department of Indian Institute of Science
Biochemistry Bangalore
Brandeis University India
Waltham, Massachusetts 02154
Michael Sela
Emanuel Margoliash Professor, Department of Chemical
Professor, Department of Biological Immunology
Sciences The Weizmann Institute of Science
Northwestern University Rehovot
Evanston, Illinois 60201 Israel
 ADVI SORY BOARD (continued)

Waclaw Szybalski Ignacio Tinoco, Jr.

Professor, McArdle Laboratory for Professor, Department of Chemistry
Cancer Research University of California
The University of Wisconsin Berkeley, California 94720
Madison, Wisconsin, 53706
Bert L. Vallee
Serge N. Timasheff
Professor, Biophysics Research
Professor, Graduate Department of Laboratory
Biochemistry
Peter Bent Brigham Hosoital
Brandeis University Harvard Medical School
Waltham, Massachusetts 02154 Boston, Massachusetts 02115
 CONT RIBUTORS

A. Acher Ralph A. Bradshaw

Laboratoire de Chemie Biologique Department of Biological Chemistry
Faculte des Sciences de Γ Division of Biology and Biomedical
Universite de Paris Sciences
Paris IV BAB 19-64 Washington University School of
France Medicine
St. Louis, Missouri 63110
K. L. Agarwal
Department of Biochemistry James R. Brown
University of Chicago Department of Chemistry
Chicago, Illinois 60637 Clayton Foundation Biochemical
Institute
R. P. Ambler The University of Texas at Austin
Department of Molecular Biology Austin, Texas 78712
King’s Buildings
University of Edinburgh Henry B. Bull
Edinburgh, EH9 3JR Department of Biochemistry
Scotland The University of Iowa
Iowa City, Iowa 52242
Winona C. Barker
National Biomedical Research Foundation
G. Chi Chen
Georgetown University Medical Center
Cardiovascular Research Institute
Washington, D. C. 20007
University of California
School of Medicine
G. H. Beaven
San Francisco, California 94122
National Institute for Medical
Research
The Ridgeway R. A. Chen
London, NW7 Public Health Service
England National Institutes of Health
Bethesda, Maryland 20853
Dennis Borden
Department of Biochemistry and
Molecular Biology Margaret O. Dayhoff
Northwestern University National Biomedical Research
Evanston, Illinois 60201 Foundation
Georgetown University Medical Center
Felix Borek Washington, D. C. 20007
Department of Microbiology
Tel-Aviv University
Richard E. Dickerson
Ramat Aviv, Tel-Aviv
Department of Chemistry
Israel
California Institute of Technology
Pasadena, California 91109
D. P. Botes
Council for Scientific and Industrial
Research Russell F. Doolittle
National Chemical Research Laboratory Department of Chemistry
Pretoria, 0001 University of California, San Diego
South Africa La Jolla, California 92037
 CONT RIBUTORS (continued)

Jan Drenth J. leuan Harris

Laboratorium voor Structuurchemie Medical Research Council
Chemische Laboratoria der Laboratory of Molecular Biology
Rijksuniversiteit Cambridge, CB2 2QH
Zernikelaan, Paddepoel, Groningen England
The Netherlands
K. Ingham
John B. R. Dunn Clinical Endocrinology Branch
Department of Chemistry and National Institute of Arthritis,
Biomedical Sciences Metabolism, and Digestive Diseases
Oregon Graduate Center National Institutes of Health
Beaverton, Oregon 97005 Bethesda, Maryland 20014

K. R. K. Easwaran
Molecular Biophysics Unit Bruno Jirgensons
Indian Institute of Science M. D. Anderson Hospital and
Bangalore, 560012 Tumor Institute
India University of Texas
Houston, Texas 77025
Peter P. Fietzek
Max-Planck Institute fur Biiochemie Andrew H. Kang
8033-Martinsreid bei University of Tennessee
Munich Center for Health Sciences
West Germany Veterans Administration Hospital
Memphis, Tennessee 38104
Joseph A. Gaily
School of Graduate Studies
Meharry Medical College Linda M. Keefer
Nashville, Tennessee 37208 Department of Biological Chemistry
Division of Biology and Biomedical
Morris Goodman Sciences
Department of Anatomy Washington University School of
Wayne State University Medicine
School of Medicine St. Louis, Missouri 63110
Detroit, Michigan 48201

Christoph de Haen Jack L. Koenig

Department of Biochemistry Department of Macromolecular
Health Science Building Science
University of Washington Case Western Reserve University
Seattle, Washington 98195 Cleveland, Ohio 44106

William F. Harrington
McCollum-Pratt Institute and Gerson Kegeles
Department of Biology Section of Biochemistry and Biophysics
The Johns Hopkins University University of Connecticut
Baltimore, Maryland 21205 Storrs, Connecticut 06268
 CONT RIBUTORS (continued)

H. Lehmann John G. Pierce

MRC Abnormal Haemoglobin Unit Department of Biological Chemistry
Department of Biochemistry School of Medicine
University of Cambridge The Center for the Health Sciences
Addenbrooke’s Hospital University of California, Los Angeles
Cambridge, CB2 2QR Los Angeles, California 90024
England
John Potts, Jr.
Joann S. Loehr Endocrine Unit
Department of Chemistry
Harvard Medical School
Portland State University
Massachusetts General Hospital
Portland, Oregon 97207
Boston, Massachusetts 02114

Thomas M. Loehr Miloslav Rechicigl, Jr.

Department of Chemistry and Office of Research and Institutional Grants
Biochemical Sciences Agency for International Development
Oregon Graduate Center Department of State
Beaverton, Oregon 97005 Washington, D. C. 20523

Rose G. Mage
Laboratory of Immunology Gerald Reeck
National Institute of Allergy and Department of Biochemistry
Infectious Diseases University of Washington
National Institutes of Health Seattle, Washington 98105
Bethesda, Maryland 20014
M. W. Rees
Emanuel Margoliasch Department of Virus Research
Department of Biochemistry and John Innes Institute
Molecular Biology Colney Lane
Northwestern University Norwich, NR4 7UH
Evanston, Illinois 60201 England

Chris Nolan
James R. Riordan
Department of Molecular Biology
Biophysics Research Laboratory
Abbott Laboratories
Peter Bent Brigham Hospital
North Chicago, Illinois 60022
Boston, Massachusetts 02115
James C. Osborne, Jr. Michael Sela
Clinical Endocrinology Branch Department of Chemical Immunology
National Institute of Arthritis, The Weizmann Institute of Science
Metabolism, and Digestive Diseases Rehovot, Israel
National Institutes of Health
Bethesda, Maryland 20014
Jerome M. Seyer
Paul C. Painter University of Tennessee
Department of Macromolecular Science Center for Health Sciences
Case Western Reserve University Veterans Administration Hospital
Cleveland, Ohio 44106 Memphis, Tennessee 38104
 CONT RIBUTORS (continued)
Gene M. Shearer Koiti Titani
Immunology Branch Department of Biochemistry
National Cancer Institute Health Science Building
National Institutes of Health University of Washington
Bethesda, Maryland 20014 Seattle, Washington 98195

Lawrence B. Smillie
J. Vanderkooi
Department of Biochemistry
The University of Alberta Johnson Research Foundation
Edmonton, T6G 2E1 University of Pennsylvania
Canada Philadelphia, Pennsylvania 19174

Donald F. Steiner Sam D. Waksal

Department of Biochemistry Immunology Branch
University of Chicago National Cancer Institute
Chicago, Illinois 60637 National Institutes of Health
Bethesda, Maryland 20014
E. Hardin Strickland
15980 Yellow Brick Road
Valley Center, California 92082 John Walker
Medical Research Council
J. Strydom Laboratory of Molecular Biology
Council for Scientific and Cambridge, CB2 2QH
Industrial Research England
National Chemical
Pretoria, 0001 Kenneth A. Walsh
South Africa Department of Biochemistry
Health Sciences Building
H. Susi University of Washington
U.S. Department of Agriculture Seattle, Washington 98195
Eastern Regional Research Center
Philadelphia, Pennsylvania 19118 R. Wojciech (deceased)

Masaru Tanaka
Department of Biochemistry and Biophysics Jen Tsi Yang
University of Hawaii Medical School Department of Biochemistry
Honolulu, Hawaii 96822 and Biophysics
Cardiovascular Research Institute
David Teller University of California
Department of Biochemistry School of Medicine
Health Science Building San Francisco, California 94122
University of Washington
Seattle, Washington 89195 Kerry T. Yasunobu
Department of Biochemistry
Russell Timkovich and Biophysics
Department of Chemistry Biomedical Sciences Building
Illinois Institute of Technology University of Hawaii at Manoa
Chicago, Illinois 60616 Honolulu, Hawaii 96822
 PREF ACE

The rapid pace at which new data is currently accumulated in science presents one of
the significant problems of today - the problem of rapid retrieval of information. The
fields of biochemistry and molecular biology are two areas in which the information
explosion is manifest. Such data is of interest in the disciplines of medicine, modern
biology, genetics, immunology, biophysics, etc., to name but a few related areas. It was
this need which first prompted CRC Press, with Dr. Herbert A. Sober as Editor, to
publish the first two editions of a modern Handbook o f Biochemistry, which made
available unique, in depth compilations of critically evaluated data to graduate students,
post-doctoral fellows, and research workers in selected areas of biochemistry.
This third edition of the Handbook demonstrates the wealth of new information
which has become available since 1970. The title has been changed to include molecular
biology; as the fields of biochemistry and molecular biology exist today, it becomes more
difficult to differentiate between them. As a result of this philosophy, this edition has
been greatly expanded. Also, previous data has been revised and obsolete material has
been eliminated. As before, however, all areas of interest have not been covered in this
edition. Elementary data, readily available elsewhere, has not been included. We have
attempted to stress the areas of today’s principal research frontiers and consequently
certain areas of important biochemical interest are relatively neglected, but hopefully not
totally ignored.
This third edition is over double the size of the second edition. Tables used from the
second edition without change are so marked, but their number is small. Most of the
tables from the second edition have been extensively revised, and over half of the data is
new material. In addition, a far more extensive index has been compiled to facilitate the
use of the Handbook. To make more facile use of the Handbook because of the increased
size, it has been divided into four sections. Each section will have one or more volumes.
The four sections are titled:

Proteins —Amino Acids, Peptides, Polypeptides, and Proteins

Nucleic Acids - Purines, Pyrimidines, Nucleotides, Oligonucleotides, tRNA, DNA,
RNA
Lipids, Carbohydrates, Steroids
Physical and Chemical Data, Miscellaneous - Ion Exchange, Chromatography,
Buffers, Miscellaneous, e.g., Vitamins

By means of this division of the data, we can continuously update the Handbook by
publishing new data as they become available.
The Editor wishes to thank the numerous contributors, Dr. Herbert A. Sober, who
assisted the Editor generously, and the Advisory Board for their counsel and cooperation.
Without their efforts this edition would not have been possible. Special acknowledgments
are due to the editorial staff of CRC Press, Inc., particularly Ms. Susan Cubar Benovich,
Ms. Sandy Pearlman, and Mrs. Gayle Tavens, for their perspicacity and invaluable assistance
in the editing of the manuscript. The editor alone, however, is responsible for the
scope and the organization of the tables.
We invite comments and criticisms regarding format and selection of subject matter, as
well as specific suggestions for new data (and their sources) which might be included in
subsequent editions. We hope that errors and omissions in the data that appear in the
Handbook will be brought to the attention of the Editor and the publisher.

Gerald D. Fasman
Editor
August 1975
 PREF ACE TO AMINO ACIDS, PEPTIDES, POLYPEPTIDES, AND
PROTEINS, VOLUME III

The section of the Handbook o f Biochemistry and Molecular Biology on Amino Acids,
Peptides, Polypeptides, and Proteins is divided into three volumes. The third volume
contains information mainly on Proteins.
Physical-chemical data on optical rotatory dispersion, circular dichroism, ultraviolet
absorption, nuclear magnetic resonance, laser raman, infrared, and fluorescence of proteins
are tabulated, e.g., oxytocin, viral coats, cytochromes, enzymes, hormones, immuno­
globulins, haemoglobins, collagen, muscle, serum albumin.
Immunochemical data, such as immunoglobin allotypes and synthetic antigens, are
made available.
The first volume contains information on amino acids, amino acid derivates, etc., and
the second volume is mainly devoted to proteins.
Although the data, for which the editor alone is responsible, is far from complete,
it is hoped that these volumes will be of assistance to those working in the field of bio­
chemistry and molecular biology.

Gerald D. Fasman
Editor
January 1976
 THE EDITOR

Gerald D. Fasman, Ph.D., is the Rosenfield Professor of Biochemistry, Graduate

Department of Chemistry, Brandeis University, Waltham, Massachusetts.
Dr. Fasman graduated from the University of Alberta in 1948 with a B.S. Honors
Degree in Chemistry, and he received his Ph.D. in Organic Chemistry in 1952 from the
California Institute of Technology, Pasadena, California. Dr. Fasman did postdoctoral
studies at Cambridge University, England, Eidg. Technische Hochschule, Zurich,
Switzerland, and the Weizmann Institute of Science, Rehovoth, Israel. Prior to moving to
Brandeis University, he spent several years at the Children’s Cancer Research Foundation
at the Harvard Medical School. He has been an Established Investigator of the American
Heart Association, a National Science Foundation Senior Postdoctoral Fellow in Japan,
and recently was a John Simon Guggenheim Fellow.
Dr. Fasman is a member of the American Chemical Society, a Fellow of the American
Association for the Advancement of Science, Sigma Xi, The Biophysical Society,
American Society of Biological Chemists, The Chemical Society (London), the New York
Academy of Science, and a Fellow of the American Institute of Chemists. He has
published 180 research papers.
The Editor and CRC Press, Inc. would like to dedicate this
third edition to the memory of Eva K. and Herbert A.
Sober. Their pioneering work on the development of the
Handbook is acknowledged with sincere appreciation.
 TABL E OF CONTENTS

PROTEINS
Optical Rotatory Dispersion and Circular Dichroism of P r o t e i n s ........................................................ 3
Near-ultraviolet Circular Dichroism Bands of Proteins .................................................................... 141
Near-ultraviolet Circular Dichroism Bands of Aromatic Amino Acids and Peptides .................... 167
Ultraviolet and Visible Absorption Spectra of Human Normal Adult Hemoglobin Derivatives and
Related C o m p o u n d s ...........................................................................................................................174
Active Site Peptides ...............................................................................................................................186
Amino Acid Sequence, Physical and Biological Properties of Natural and Related Synthetic
Oligopeptides - Oxytocin and Vasopressin Group .................................................................... 192
Amino Acid Sequence, Physical and Biological Properties of Natural and Related Synthetic
Oligopeptides - Bradykinin and Kallidin Group ........................................ ................................221
Amino Acid Sequence, Physical and Biological Properties of Natural and Related Synthetic
Oligopeptides —Eledoisin and Physalaemin Group .................................................................... 236
Amino Acid Sequences of Proteins - Coat Proteins .............................................. 261
Amino Acid Sequences of Virus Coat Proteins (Turnip Yellow Mosaic Virus, T Y M ) .....................263
Location of Some Amino Acid Replacements in Naturally Occurring (NM) and Chemically
Induced (CM) Mutants of TMV .................................................................................................... 266
Amino Acid Sequences of Proteins —Eukaryotic Cytochromes c .................................................268
Amino Acid Sequences of Proteins —Eukaryotic and Prokaryotic Cytochromes b .....................280
Amino Acid Sequences of Eukaryotic Cytochromes c ...................................................................... 282
Frequency of Occurrence of Amino Acids Among 60 Species at Different Positions Along
Chain ...................................................................................................................................................288
Amino Acid Sequences of Prokaryotic Cytochromes c .................................................................... 292
Amino Acid Sequences of Proteins - E n z y m e s .................................................................. .3 0 8
Amino Acid Sequences of Proteins —Pyridine Nucleotide-dependent D ehydrogenases.................314
Amino Acid Sequence of T herm olysin.................................................................................................. 322
Amino Acid Sequences of Gastrins .....................................................................................................323
List of Complete Sequences of Glycolytic E n z y m e s ........................................................................ 324
Bovine Carboxypeptidase B and A ............................................................................................ 338
Amino Acid Sequence Data on Trypsin-related Serine P r o te a s e s .................................................... 340
Amino Acid Sequences of Papain, Stem Bromelain, Fruit Bromelain, Ficin, Chymopapain-B, and
Streptococcal Proteinase . : .......................................................................................................... 356
The Complete Amino Acid Sequence of Porcine Pepsin ................................................................ 358
Homology in Sequences Adjoining the Trypophanyl and Active Center Aspartyl Residues
in P e p s i n ...............................................................................................................................................359
Snake Venom T o x i n s ...............................................................................................................................360
Amino Acid Sequences of Proteins —Hormones .............................................................................. 375
Amino Acid Sequences of Proteins —Hormones (Insulins) .............................................................. 378
Sequences of Calcitonins .......................................................................................................................383
Amino Acid Sequences of Proteins —Hormones of the Anterior Pituitary and Placenta . . . . 385
Amino Acid Sequences of Parathyroid H o r m o n e s ........................................................ 399
Distribution of Neurohypophysial Hormones in Vertebrates .......................................................... 400
Structures of Neurohypophysial Hormones of V e te b ra te s.................................................................. 401
The Amino Acid Sequence of Human Chorionic Gonadotropin ................................ ....................402
Amino Acid Sequences of Immunoglobulins ............................................................................ . 403
Amino Acid Sequence of some Proteins —Ferredoxins .....................................................................421
Amino Acid Sequences of Proteins —Fibrinopeptides ................ ' .................................................. 431
Amino Acid Sequences of Proteins —Vertebrate Myoglobins .......................................................... 437
Amino Acid Sequences of Proteins —a. Type Chains of Vertebrate Tetrameric Hemoglobins . .441
Amino Acid Sequences of Proteins —β Type Chains of Vertebrate Tetrameric Hemoglobins . . 448
 Amino Acid Sequences of Proteins —Aligned Chains of Metazoan Globins and Soybean
Leghemoglobin.......................................................................................................................................456
List of Known Hemoglobin Substitutions and Deletions ................................................................ 461
Amino Acid Sequences of Collagen C h a i n s .........................................................................................474
Amino Acid Sequences of the Muscle Contractile Proteins ............................................................ 490
Bovine Serum A lb u m in ..................................................... ' ............................................................... 497
Human Serum A lb u m in ...........................................................................................................................498
Amino Acid Sequences of Proteins —M iscellan e o u s.........................................................................499
Mamallian α-Crystallin A Chains ...........................................................................................................503
Amino Acid Compositions of Selected P r o t e i n s .................................................................................504
Selected Amino Acid Analysis of C ollagens...........................................................................................520
Cross-linkages in C o lla g e n .......................................................................................................................523
Post-translational Enzymes in Collagen . : . . .............................................................................524
Immunoglobulins of Laboratory Animals ...........................................................................................525
Some Properties of Human Im m unoglobulins.......................................................................................528
Disulfide Bonding Patterns of Immunoglobin Molecules .................................................................. 529
Immunoglobulin Allotypes ...................................................................................................................530
Cell Types Involved in Immunological Response .............................................................................536
Some Low Molecular Weight Compounds with Immunogenic Properties .................................... 541
Methods for Detection of Antibody-producing C e l l s ...........................................................................542
Methods for Detection of Serum A n tib o d ie s .....................................................................................543
Immunogenic Synthetic P o ly p e p tid e s................................................................................................... 546
Immunogenic Peptides and their Derivatives .......................................................................................549
Immunogenic Conjugates of Synthetic P o ly p e p tid e s .......................................................................... 550
Molecular Turnover of Enzymes in Animal Tissues ......................................................................... 552
Molecular Turnover of Cytochromes in A n im a ls.................................................................................559
Proton Magnetic Resonance Spectral Data and Suggested Conformations of Biologically Active
Cyclic Peptides and Cyclic Peptide A n tib io tic s .............................................................................560
Raman Spectroscopy of Polypeptides and Proteins .......................................................................... 575
Resonance Raman Spectra of P r o te in s ...................................................................................................588
Volume Changes for Some Macromolecule Association Reactions ............................ 593
Temperature Coefficients of Apparent Partial Specific Volumes of Proteins Expressed in ml/g/deg
( d V / d T ) ...............................................................................................................................................595
Infrared Spectra of P r o t e i n s ...................................................................................................................596
Fluorescent Enzyme In h ib ito rs ...............................................................................................................598
Fluorescence of Enzyme C o f a c to r s ...................................................................................................... 601
Fluorescent Probes of Protein Structure: Naphthalene Sulfonates .................................................. 604
Properties of Fluorescent Probes Commonly Used for Membrane S t u d i e s .................................... 608

INDEX . 613
Proteins
 3

OPTICAL ROTATORY DISPERSION AND CIRCULAR DICHROISM

OF PROTEINS*

Jen Tsi Yang, G. Chi Chen, and Bruno Jirgensons

Biot in 1836 introduced the term specific rotation, [a], for the optical activity of a
compound1"3

( 1)

where

a = the observed rotation of the plane of polarized light in angular degrees at

wavelength X;
β = the optical path in decimeters;
c = the concentration of the compound in grams per milliliter.

The dimension is deg cm2 decagram"1. The traditional use of specific rotation at sodium
D line, [a] is now obsolete with the availability of modern spectropolarimeters. Here D
refers to 589 nm and t the temperature in centigrade.
For biopolymers, the data are usually expressed in terms of mean residue rotation,
[m]

[m] = (Mo /1 0 0 )[a ] (2)

where M0 is the mean residue (molecular) weight. (Some workers prefer the symbols [φ]
or [R] for [m] and MRW for M0.) M0 of a protein can be determined from its amino
acid composition (for most proteins, M0 = 115). Moffitt4 introduced the term reduced
mean residue rotation, [m '], by including a Lorentz field correction

[ml = [m][3/(n2 +2)] (3)

which reduces [m] to that under vacuum, noting that the refractive index is unity in
vacuum. The dimension of both [m] and [m;] is deg cm2 dmol-1 .
Optical rotatory dispersion (ORD) in the visible region of most proteins obeys the
Drude equation

(4)

where Xc and k are the dispersion and rotatory coefficients. A plot of λ 2 [a] χ vs. [a] χ
yields a straight line with Xc2 as the slope and k as the intercept (at [α] χ = 0).5 The
Moffitt equation for α-helical polypeptides4

♦The survey o f literature pertaining to this section was completed through December 1974. This work
was aided by USPHS grants HL-06285 and GM-10880 and grant G-051 from the R. A. Welch
Foundation, Houston, Texas. Technical assistance by Ms. C. Ue and Mrs. L. Matsushima is
is acknowledged.
4 Handbook o f Biochemistry and Molecular Biology

has now replaced the Drude equation for the ORD of proteins (except collagen). By
rearranging Equation 5 into

(6)

the b0 and a0of a protein can be determined from a plot of [in ](λ 2/λο2 - 1) vs.
1/(λ2/λ02 - 1) with Xq usually preset at 212 nm. A b0 o f -630 deg cm2 dmol-1 , based
on the data of synthetic polypeptides, is regarded to represent a perfect helix. The
Moffitt equation, now considered to be empirical, still provides a reasonable estimate of
the helical content in a protein molecule. Both Equations 4 and 5 are only applicable over
a certain wavelength range. Often a λ0 larger than 212 nm must be used when the data
below 300 to 350 nm are included for the fitting of the Moffitt equation. For the
convenience of comparison, we will list only the ao and b0 values based on λ0 =212 nm
(with a few exceptions).
The visible ORD can also be fitted with many two-term Drude equations

(7 )

One such equation has been proposed by Shechter and Blout6 with λι = 193 and λ2 =
225 nm. All these equations can be reduced to the Moffitt equation.7
Circular dichroism (CD) is the difference in molar (or mean residue) absorptivities, (eL
- eR), between the left- and right-handed circularly polarized components of a linearly
polarized light. Since the emergent light becomes elliptically polarized, CD can also be
expressed in terms of molar (or mean residue) ellipticity. In analogy to optical rotation,
specific ellipticity, [φ ], is defined as

(8 )

and mean residue ellipticity as

(9 )

Since the absorbance (or optical density), A, is related to e by

( 10)

where m is the concentration in moles per liter and the light path in centimeters, it can
be shown that3

(11)

and
( 12)

or
( 13)

The Roussel-Jouan circular dichrograph measures directly (AL - AR), which can be
converted into (eL - eR) (Equation 10) or [0] (Equation 12). On the other hand, the
JASCO and Cary 61 instruments measure the ellipticity, ψ, in degrees. [0] can be
calculated from Equations 8 and 9. Most workers seem to prefer [0] over (eL - eR), but
these two quantities are interconvertible according to Equation 13. The dimension of [0]
is again deg cm2 dmol_1.
 5

An important theoretical quantity is the rotational strength, R, of a CD band,

although rarely reported in the biochemical literature. It is R that determines both the
sign and magnitude of the ellipticity. For an i-th band, it is related to the experimental
ellipticity by8

(14)

For a Gaussian CD band, Equation 14 reduces to

(15)

where [0°^ is the extremum of [0J at λ Ό[ and Δ°ί is the half-band width.
ORD is a dispersive and CD an absorptive property. They are interrelated by the
general Kronig-Kramers transform.8

(16)

and
(17)

Computer programs have made solutions of Equations 16 and 17 easy.9 A CD band and
its corresponding ORD in the region of the absorption band is often called a Cotton
effect, as distinguished from the featureless ORD away from the absorption band.
For a Gaussian CD band, Equation 16 becomes

(18)

where c = (λ - λ°ί)/λ°ί· The numerical values of the function e °2/ο eX dx are listed in
Table 1. As c goes to ± °°, Equation 18 reduces to a simple Drude equation

(19)

The CD and ORD of a helix, j3-form, and aperiodic form all display their
characteristic Cotton effects (Figures 1 and 2).* The magnitudes of the spectra for the
helix in the 220- to 250-nm region overshadow those of the other two conformations.
The appearance of a double CD minimum at 222 and 208 to 210 nm usually indicates the
presence of helices. The magnitudes of [0 ) 2 2 2 and also [m] 2 3 3 have been used for
estimating the percent of helix in a protein molecule. Collagen is a notable exception,
which forms a triple helix unlike the above-mentioned three conformations. Its CD and
ORD are illustrated in Figure 3.
From the middle 1950’s to early 1960’s almost all the data of optical activity of
proteins were confined to ORD in the visible and near UV (above 300 nm) regions
because of the instrumental limitations. They were usually fitted with the Moffitt or
Drude equation. Now the Cotton effects in the UV region are widely used for studying
protein conformations. Since CD can identify individual bands of various conformations,
it appears to gain on ORD in its use even though the two measurements are
complementary to each other. The current commercial instruments have a cutoff near
184 nm, but recent vacuum UV CD developments have extended the measurements to
about 160 nm in aqueous solutions and about 140 nm for films (Figure 4).

*Figures 1 - 1 0 follow text.

6 Handbook o f Biochemistry and Molecular Biology

Since not every protein studied has a complete set of CD and ORD, we will divide the
literature data into three tables. Table 2 covers the Moffitt parameters based on the
visible ORD; Tables 3 and 4 list the magnitudes of the extrema of ORD and CD in the UV
region, respectively. Because of limitation of space, only native proteins in aqueous
solutions (with a few exceptions) are compiled in this work. Usually only one set of data
for each protein is listed with additional references for similar results. (The choice is by
necessity arbitrary, and it is not our intention to favor any one paper over the other.)
Since the signal-to-noise ratio decreases markedly at wavelengths below 200 nm, the*
precision of the data in this region should be viewed with some caution. Occasionally,
more than one set of data is listed for a particular protein mainly because of large
discrepancies among the literature values.
About two thirds of the data listed in Tables 2, 3, and 4 have been verified by the
original authors, thanks to their generous cooperation. One possible source of error was
the numerous methods used for determining the concentrations of proteins; as such,
information provided by the authors on concentration determination is included in the
tables. Another uncertainty is the correct value of mean residue weight, M0, which could
vary from 100 to 130. Unless M0 has been calculated from the amino acid composition of
the proteins, the use of an average M0 = 115 could affect the accuracy of the listed
values.
The Lorentz correction factor for converting [m] into [m] (Equation 3) is of
historical interest but questionable practical value. At most, it accounts for a crude gross
aspect of the solvent effect; for instance, the core of a protein molecule will experience a
different microenvironment from that of the surface of the molecule. If such a refractive
index correction is applied to CD, the factor would have been 9n/(n2 + 2)2 rather than
3/(n2 + 2).10 In any case, this correction becomes unnecessary if our interest is only to
compare the conformations of various proteins in aqueous solutions. Following tradition,
many workers still prefer to report [m*] instead of [m]. On the other hand, almost all
CD data are expressed either in eL - eR or [Θ] without the Lorentz correction. To
compromise this unusual situation, we list both [m'] and [m] in Table 3 if the former is
listed in the original literature. The reasons are twofold. First, some authors object to any
changes of their published values. Second, refractive index, n, is wavelength dependent. It
is not known whether the correct n value wavelength for wavelength (a tedious task in
itself) or only an average n value such as that at sodium D line was used. Thus, in a
footnote to Table 3, we specify the correction factor used for converting [m] back to
[m] so as to avoid any possible confusion, unless the authors have specified otherwise.
For the b0 and a0 values of the Moffitt equation (Table 2), we retain the refractive index
correction factor mainly because they have been so deep-rooted that any change in
definition at this stage would merely cause unavoidable confusion. We hope that in future
editions the workers in this field will have agreed on a set of terms such as [m] and [0].
Only three significant figures are listed in the tables, although some authors have reported
four figures.
Figures 5 and 6 illustrate a typical protein containing a high helical content and a large
amount of j3-form, respectively. Figure 7 shows an atypical protein whose CD spectrum
resembles none of the three conformations or their combinations. For conjugated
proteins, the nonprotein moieties can contribute to the optical activity of the complexes,
in particular, the nucleic acids and, to a lesser extent, the lipids and carbohydrates.
Figures 8 and 9 illustrate two such CD spectra. How to separate their contributions from
those of proteins remains a problem. This is especially serious for ORD spectra, since the
CD bands in the far UV region can still contribute, to rotations in the near UV and visible
regions. Solutions of proteins with strong light scattering (e.g., biomembranes) have
shown CD spectra of reduced magnitude accompanied by red shifts in band positions.
 7

Several theoretical treatments have been proposed, and the subject is still open to
intensive investigations.
At present, the CD and ORD spectra of proteins are used for analyzing the three
known conformations. Assuming the additivity of the optical activity, we have at any
chosen wavelength, λ,

( 20 )

Here X can be either [Θ] or [m]. The XH, X^, and XR are the reference values of the
helix (Η), β- and aperiodic (R) form. The fs are the fractions of the three forms in a
protein molecule. With known reference values, the f s can be solved from a series of
simultaneous equations such as Equation 20, one for each wavelength, by the method of
least squares. There are two schools about the choice of the reference values. One uses
synthetic polypeptides as the model compound for the three forms11 and the other
computes the reference values from the CD (or ORD) spectra of proteins of known
three-dimensional structure.12 In the latter case, the chain-length dependence of the
optical activity of helices (Figure 10) can provide an additional estimate of the average
number of helical segments and residues per segment in a protein molecule, although the
method is not yet perfected (for details, see Reference 12). Tables 5 and 7 list the
reference values for CD at 1-nm intervals and Tables 6 and 8 for ORD that are currently
used. The method of analysis based on Equation 20 appears to work reasonably well for
proteins containing at least a moderate amount of helices.
Cotton effects of nonpeptide chromophores would of course complicate the above
methods of analysis. In most cases the Cotton effects due to aromatic groups and
disulfide linkages appear to be small as compared with those of peptide chromophores
and are often overlooked in the analysis, which naturally introduces some uncertainties.
8 Handbook o f Biochemistry and Molecular Biology

FIGURE 1. Circular dichroism (A) and optical rotatory dispersion (B) o f the helix (H), β, and unordered (R) form
based on synthetic polypeptides. Curves Η, β, and R for poly(L-lysine) in water: H at pH 11.1; β at pH 11.1 after 15 min
heating at 52°C and cooling back to 22°C; R, unordered at pH 5.7. [Redrawn with permission from Greenfield and
Fasman, B io ch em istry, 8, 4108 (1969); Greenfield, Davidson, and Fasman, B ioch em istry, 6, 1630 (1967). Copyright
by the American Chemical Society.) Curve 0':0-poly( L-ly sine) in 1% sodium dodecyl sulfate at neutral pH. [Redrawn
with permission from Li and Spector, /. A m . Chem. Soc., 9 1 ,2 2 0 (1969). Copyright by the American Chemical Society.)
Curve R': unordered poly(L-serine) in 8 M LiCl. [Reprinted with permission from Quadrifoglio and Urry, J. A m . Chem.
Soc., 90, 2760 (1968). Copyright by the American Chemical Society.)
 9

FIGURE 2. Circular dichroism (A) and optical rotatory dispersion (B) o f the helix (H), 0, and unordered
(R) form computed from the corresponding spectra o f five proteins (myoglobin, lysozym e, lactate dehydro­
genase, papain, and ribonuclease). [Reprinted with permission from Chen, Yang, and Chau, B io ch em istry ,
13, 3350 (1974). Copyright by the American Chemical Society.]
 10

FIGURE 3. Circular dichroism (A) o f rat tail collagen in the native and
denatured states in aqueous solution. [Redrawn from Tiffany and Krimm, B io ­
p o lym e rs, 8, 347 (1969). Reprinted by permission o f John Wiley & Sons, Inc.]
H a n d b o o k o f B io ch em istry a n d M olecular B io lo g y

Optical rotatory dispersion (B) o f calf thymus collagen in the native and FIGURE 4. Vacuum UV circular dichroism o f poly(7-methyl-L-
denatured states in 0.01 M acetic acid solution. [Redrawn with permission from glutamate) in hexafluoro-2-propanol. [Redrawn with permission from
Blout, Carver, and Gross, J. A m . Chem . Soc., 85, 644 (1963). Copyright by the Johnson and Tinoco, J. A m . Chem. Soc., 94, 4389 (1972). Copyright
American Chemical Society.] by the American Chemical Society.]

FIGURE 5. (at right) A protein con­

taining a high helical content: tropo­
myosin in 0.04 M sodium pyrophos­
phate. (From Wu, unpublished data.)
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{705}

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August 31, 1897.

Speech by the German Emperor at Coblenz, asserting
"kingship by the grace of God," with "responsibility to the
Creator alone."
Death of Mrs. Louisa Lane Drew, actress.

September 10, 1897.

Death of Theodore Lyman, American naturalist.

September 11, 1897.

Death of Reverend Abel Stevens,
 American historian of the Methodist church.

September 12, 1897.

Ending of a great strike of coal miners in the United States,
which began in July.

September 16, 1897.

Death of Edward Austin Sheldon, American educator.

September 17, 1897.

Death of Henry Williams Sage, American philanthropist.

September 18, 1897.

Signing of a preliminary treaty of peace
between Turkey and Greece.

September 20, 1897.

Death of Wilhelm Wattenbach, German historian.

September 22, 1897.

Meeting at Washington of a commission on monetary reform,
appointed by the Indianapolis Convention of January 12.
Death of Charles Denis Sauter Bourbaki, French general.

September 28, 1897.

Vote on proposed constitutional amendments in New Jersey.

October 1, 1897.
Introduction of the gold monetary standard in Japan.

October 2, 1897.
Death of Neal Dow, American temperance reformer.

October 4, 1897.
Death of Professor Francis William Newman,
English scholar and philosopher.
October 6, 1897.
The Philippine Islands swept by a typhoon,
destroying over 6,000 lives.
Death of Sir John Gilbert, English artist.

October 18, 1897.

Death of Rear-Admiral John Lorimer Worden, U. S. N.

October 19, 1897.

Death of George Mortimer Pullman, American inventor.

October 21, 1897.

Opening and dedication of the Yerkes Observatory,
at Williams Bay, Wisconsin.

October 22, 1897.

Death of Justin Winsor, American historian and bibliographer.

October 24, 1897.

Death of Francis Turner Palgrave, English poet.

October 25, 1897.

Death of John Sartain, American artist.
Death of John Stoughton, English church historian.

October 27, 1897.

Death of Mary, Duchess of Teck.
Death of Alexander Milton Ross, Canadian naturalist.

{708}

October 28, 1897.

Stormy session of the Austrian Reichsrath; twelve-hours'
speech of Dr. Lecher.
Death of Hercules George Robinson, Baron Rosmead,
British colonial administrator.
October 29, 1897.
Death of Henry George, American economist.

November 2, 1897.
Election of the first Mayor of "Greater New York."
Death of Sir Rutherford Alcock, British diplomatist.

November 4, 1897.
Seizure by Germany of the port of Kiao-chau on the
northeastern coast of China.

November 6, 1897.
Signing of treaty between Russia, Japan and the United States,
providing for a suspension of pelagic sealing.

November 10, 1897.

Adoption of plans for a building for the
New York Public Library.

November 14, 1897.

Death of Thomas Williams Evans, American dentist in Paris,
founder of the Red Cross Society in the Franco-Prussian war.

November 15, 1897.

Commandant Esterhazy denounced to the French Minister of War,
by M. Matthieu Dreyfus, as the author of the "bordereau" on
which Captain Alfred Dreyfus was secretly convicted.

November 16, 1897.

The Dreyfus case brought into the French Chamber of Deputies
by a question to the Minister of War.

November 19, 1897.

Great fire in London, beginning in Aldersgate and spreading
over six acres, destroying property estimated at £2,000,000
in value.
Death of Henry Calderwood, Scottish philosopher.
November 21, 1897.
Death of Sir Charles Edward Pollock, English jurist.

November 23, 1897.

Death of A. Bardoux, French statesman.

November 25, 1897.

Promulgation by royal decree at Madrid of a constitution
establishing self-government in Cuba and Porto Rico.

November 29, 1897.

Death of James Legge, Scotch oriental scholar.

December, 1897.
Annexation of Zululand to Natal Colony.

December 5, 1897.
Death of Mrs. Alice Wellington Rollins, American author.

December 14.
Signing of the treaty of Biac-na-bato, between the Spaniards
and the insurgent Filipinos.

December 29, 1897.

Approval of Act of Congress forbidding the killing of seals
by citizens of the United States, in the Pacific Ocean north
of 35° North latitude.
Death of William James Linton, American artist and author.

December 31, 1897.

Imperial proclamation, closing the sittings of the Austrian
Reichsrath, and continuing the Austro-Hungarian "Ausgleich"
provisionally for six months.

1898.
January 2, 1898.
Death of Sir Edward Augustus Bond, formerly principal
librarian of the British museum.

January 12, 1898.

Acquittal of Commandant Esterhazy, after a farcical pretense
of trial by a military tribunal, on the charge of being the
author of the "bordereau" ascribed to Dreyfus.

January 13, 1898.

Publication in Paris of a letter by M. Zola, denouncing the
conduct of the courts martial in the cases of Dreyfus and
Esterhazy.
Death of Mrs. Mary Victoria Cowden Clarke.

January 16, 1898.

Death of Charles Pelham Villiers, English statesman.

January 18, 1898.

Death of Henry George Liddell, English historian and
classical scholar.

January 20, 1898.

Second meeting of monetary convention at Indianapolis, to
consider the report of its commission.

January 24, 1898.

Declaration by Count von Bülow, in the German Reichstag, that
no relations or connections of any kind had ever existed
between Captain Dreyfus and any German agents.

January 25, 1898.

Friendly visit of the United States battle ship "Maine" to
Havana, Cuba.

January 28, 1898.

End of a great strike and lockout in the British engineering